Antiangiogenic therapy improves the antitumor effect of adoptive cell immunotherapy by normalizing tumor vasculature

Medical Oncology

Volumn 30, Issue 4, 2013, Pages

  Shi, Shujing ^a   Chen, Longbang ^a   Huang, Guichun ^a  

^a MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

Author keywords

Abnormal tumor vasculature; Adoptive cell immunotherapy; Hypoxia inducible factor; Hypoxic tumor microenvironment

Indexed keywords

ANTINEOPLASTIC AGENT; HYPOXIA INDUCIBLE FACTOR 1; MONOCLONAL ANTIBODY DC101; VASCULOTROPIN INHIBITOR; ANGIOGENESIS INHIBITOR;

ADOPTIVE IMMUNOTHERAPY; ANTIANGIOGENIC THERAPY; ANTINEOPLASTIC ACTIVITY; ARTICLE; DENDRITIC CELL; HUMAN; HYPOXIA; IMMUNOLOGICAL TOLERANCE; MATURATION; MYELOID DERIVED SUPPRESSOR CELL; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; SUPPRESSOR CELL; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR VASCULARIZATION; ANIMAL; METHODOLOGY; MULTIMODALITY CANCER THERAPY; NEOVASCULARIZATION (PATHOLOGY); REVIEW;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS; COMBINED MODALITY THERAPY; HUMANS; IMMUNOTHERAPY, ADOPTIVE; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 84882550346     PISSN: 13570560     EISSN: 1559131X     Source Type: Journal    
DOI: 10.1007/s12032-013-0698-1     Document Type: Article

References (55)

1. Prieto PA, Yang JC, Sherry RM, Hughes MS, Kammula US, White DE, Levy CL, Rosenberg SA, Phan GQ. CTLA-4 blockade with ipilimumab: long-term follow-up of 177 patients with metastatic melanoma. Clin Cancer Res. 2012;18:2039-47.
2. Hiscox S, Barrett-Lee P, Nicholson RI. Therapeutic targeting of tumor-stroma interactions. Expert Opin Ther Targets. 2011;15:609-21.
3. Cavallo F, De Giovanni C, Nanni P, Forni G, Lollini PL. The immune hallmarks of cancer. Cancer Immunol Immunother. 2011;60:319-26.
4. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646-74.
5. Zheng YW, Li RM, Zhang XW, Ren XB. Current adoptive immunotherapy in non-small cell lung cancer and potential influence of therapy outcome. Cancer Invest. 2013;31:197-205.
6. Padera TP, Stoll BR, Tooredman JB, Capen D, di Tomaso E, Jain RK. Pathology: cancer cells compress intratumour vessels. Nature. 2004;427(6976):695. (Pubitemid 38294577)
7. Chouaib S, Messai Y, Couve S, Escudier B, Hasmim M, Noman MZ. Hypoxia promotes tumor growth in linking angiogenesis to immune escape. Front Immunol. 2012;3:21.
8. Benito J, Shi Y, Szymanska B, Carol H, Boehm I, Lu H, Konoplev S, Fang W. Pronounced hypoxia in models of murine and human leukemia: high efficacy of hypoxia-activated prodrug PR-104. PLoS ONE. 2011;6(8):e23108.
9. Kapsenberg ML. Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol. 2003;3:984-93. (Pubitemid 37521540)
10. Moser M, Murphy KM. Dendritic cell regulation of TH1-TH2 development. Nat Immunol. 2000;1:199-205.
11. Yang M, Ma C, Liu S, Sun J, Shao Q, Gao W, Zhang Y, Li Z, Xie Q, Dong Z, Qu X. Hypoxia skews dendritic cells to a T helper type 2-stimulating phenotype and promotes tumor cell migration by dendritic cell-derived osteopontin. Immunology. 2009;128:e237-49.
12. Novitskiy SV, Ryzhov S, Zaynagetdinov R, Goldstein AE, Huang Y, Tikhomirov OY, Blackburn MR, Biaggioni I, Carbone DP, Feoktistov I, Dikov MM. Adenosine receptors in regulation of dendritic cell differentiation and function. Blood. 2008;112:1822-31.
13. Yang M, Ma C, Liu S, Shao Q, Gao W, Song B, Sun J, Xie Q, Zhang Y, Feng A, Liu Y, Hu W, Qu X. HIF-dependent induction of adenosine receptor A2b skews human dendritic cells to a Th2-stimulating phenotype under hypoxia. Immunol Cell Biol. 2010;88:165-71.
14. Pagès F, Galon J, Dieu-Nosjean MC, Tartour E, Sautès- Fridman C, Fridman WH. Immune infiltration in human tumors: a prognostic factor that should not be ignored. Oncogene. 2010;29:1093-102.
15. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pagès C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoué F, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH, Pagès F. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006;313:1960-4. (Pubitemid 44498003)
16. Pagès F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, Mlecnik B, Kirilovsky A, Nilsson M, Damotte D, Meatchi T, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH, Galon J. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med. 2005;353:2654-66. (Pubitemid 41817714)
17. Laurent C, Müller S, Do C, Al-Saati T, Allart S, Larocca LM, Hohaus S, Duchez S, Quillet-Mary A, Laurent G, Brousset P, Valitutti S. Distribution, function, and prognostic value of cytotoxic T lymphocytes in follicular lymphoma: a 3-D tissue-imaging study. Blood. 2011;118:5371-9.
18. Zuckerberg AL, Goldberg LI, Lederman HM. Effects of hypoxia on interleukin-2 mRNA expression by T lymphocytes. Crit Care Med. 1994;22:197-203. (Pubitemid 24061640)
19. Kim H, Peng G, Hicks JM, Weiss HL, Van Meir EG, Brenner MK, Yotnda P. Engineering human tumor-specific cytotoxic T cells to function in a hypoxic environment. Mol Ther. 2008;16:599-606. (Pubitemid 351315001)
20. Ohta A, Gorelik E, Prasad SJ, Ronchese F, Lukashev D, Wong MK, Huang X, Caldwell S, Liu K, Smith P, Chen JF, Jackson EK, Apasov S, Abrams S, Sitkovsky M. A2A adenosine receptor protects tumors from antitumor T cells. Proc Natl Acad Sci U S A. 2006;103:13132-7. (Pubitemid 44338928)
21. Shi S, Wang R, Chen Y, Song H, Chen L, Huang G. Combining antiangiogenic therapy with adoptive cell immunotherapy exerts better antitumor effects in non-small cell lung cancer models. PLoS ONE. 2013;. doi: 10.1371/journal.pone. 0065757.
22. Chinnasamy D, Yu Z, Theoret MR, Zhao Y, Shrimali RK, Morgan RA, Feldman SA, Restifo NP, Rosenberg SA. Gene therapy using genetically modified lymphocytes targeting VEGFR-2 inhibits the growth of vascularized syngenic tumors in mice. J Clin Invest. 2010;120:3953-68.
23. Fukumura D, Jain RK. Tumor microvasculature and microenvironment: targets for anti-angiogenesis and normalization. Microvasc Res. 2007;74:72-84. (Pubitemid 350051025)
24. Dirkx AE, oude Egbrink MG, Castermans K, van der Schaft DW, Thijssen VL, Dings RP, Kwee L, Mayo KH, Wagstaff J, Bouma-ter Steege JC, Griffioen AW. Anti-angiogenesis therapy can overcome endothelial cell anergy and promote leukocyte-endothelium interactions and infiltration in tumors. FASEB J. 2006;20:621-30. (Pubitemid 44933306)
25. Palazón A, Aragonés J, Morales-Kastresana A, de Landázuri MO, Melero I. Molecular pathways: hypoxia response in immune cells fighting or promoting cancer. Clin Cancer Res. 2012;18:1207-13.
26. Marigo I, Dolcetti L, Serafini P, Zanovello P, Bronte V. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol Rev. 2008;222:162-79. (Pubitemid 351430364)
27. Zhang B, Wang Z, Wu L, Zhang M, Li W, Ding J, Zhu J, Wei H, Zhao K. Circulating and tumor-infiltrating myeloid-derived suppressor cells in patients with colorectal carcinoma. PLoS ONE. 2013;8:e57114.
28. Yu J, Du W, Yan F, Wang Y, Li H, Cao S, Yu W, Shen C, Liu J, Ren X. Myeloid-derived suppressor cells suppress antitumor immune responses through IDO expression and correlate with lymph node metastasis in patients with breast cancer. J Immunol. 2013;190:3783-97.
29. Suresh KG, Lugade AA, Miller A, Iyer R, Thanavala Y. Higher frequencies of GARP + CTLA-4 + Foxp3 + T regulatory cells and myeloid-derived suppressor cells in hepatocellular carcinoma patients are associated with impaired T cell functionality. Cancer Res. 2013;73:2435-44.
30. Xu J, Escamilla J, Mok S, David J, Priceman SJ, West BL, Bollag G, McBride WH, Wu L. CSF1R signaling blockade improves the efficacy of radiotherapy in prostate cancer. Cancer Res. 2013;73:2782-94.
31. Christiansson L, Söderlund S, Svensson E, Mustjoki S, Bengtsson M, Simonsson B, Olsson-Strömberg U, Loskog AS. Increased level of myeloid-derived suppressor cells, programmed death receptor ligand 1/programmed death receptor 1, and soluble CD25 in Sokal high risk chronic myeloid leukemia. PLoS ONE. 2013;. doi: 10.1371/journal.pone.0055818.
32. Corzo CA, Condamine T, Lu L, Cotter MJ, Youn JI, Cheng P, Cho HI, Celis E, Quiceno DG, Padhya T, McCaffrey TV, McCaffrey JC, Gabrilovich DI. HIF-1α regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med. 2010;207:2439-53.
33. Mukhtar RA, Nseyo O, Campbell MJ, Esserman LJ. Tumor-associated macrophages in breast cancer as potential biomarkers for new treatments and diagnostics. Expert Rev Mol Diagn. 2011;11:91-100.
34. Laoui D, Movahedi K, Van Overmeire E, Van den Bossche J, Schouppe E, Mommer C, Nikolaou A, Morias Y, De Baetselier P, Van Ginderachter JA. Tumor-associated macrophages in breast cancer: distinct subsets, distinct functions. Int J Dev Biol. 2011;55:861-7.
35. Tang X. Tumor-associated macrophages as potential diagnostic and prognostic biomarkers in breast cancer. Cancer Lett. 2013;332:3-10.
36. Lan C, Huang X, Lin S, Huang H, Cai Q, Wan T, Lu J, Liu J. Expression of M2-polarized macrophages is associated with poor prognosis for advanced epithelial ovarian cancer. Technol Cancer Res Treat. 2013;12:259-67.
37. Zhang QW, Liu L, Gong CY, Shi HS, Zeng YH, Wang XZ, Zhao YW, Wei YQ. Prognostic significance of tumor-associated macrophages in solid tumor: a meta-analysis of the literature. PLoS ONE. 2012;7:e50946.
38. Lewis JS, Landers RJ, Underwood JC, Harris AL, Lewis CE. Expression of vascular endothelial growth factor by macrophages is up-regulated in poorly vascularized areas of breast carcinomas. J Pathol. 2000;192:150-8.
39. Murdoch C, Giannoudis A, Lewis CE. Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues. Blood. 2004;104:2224-34. (Pubitemid 39331817)
40. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005;307:58-62. (Pubitemid 40093472)
41. Geva R, Vecchione L, Tejpar S, Piessevaux H, Van Cutsem E, Prenen H. Bevacizumab plus chemotherapy as salvage treatment in chemorefractory patients with metastatic colorectal cancer. Onco Targets Ther. 2013;6:53-8.
42. Jain RK. Delivery of novel therapeutic agents in tumors: physiological barriers and strategies. J Natl Cancer Inst. 1989;81:570-6. (Pubitemid 19104487)
43. Goel S, Duda DG, Xu L, Munn LL, Boucher Y, Fukumura D, Jain RK. Normalization of the vasculature for treatment of cancer and other diseases. Physiol Rev. 2011;91:1071-121.
44. Jain RK. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat Med. 2001;7:987-9. (Pubitemid 32937367)
45. Huang Y, Yuan J, Righi E, Kamoun WS, Ancukiewicz M, Nezivar J, Santosuosso M, Martin JD, Martin MR, Vianello F, Leblanc P, Munn LL, Huang P, Duda DG, Fukumura D, Jain RK, Poznansky MC. Vascular normalizing doses of antiangiogenic treatment reprogram the immunosuppressive tumor microenvironment and enhance immunotherapy. Proc Natl Acad Sci U S A. 2012;109:17561-6.
46. Huang G, Chen L. Recombinant human endostatin improves anti-tumor efficacy of paclitaxel by normalizing tumor vasculature in Lewis lung carcinoma. J Cancer Res Clin Oncol. 2010;136:1201-11.
47. Huang G, Chen L. Tumor vasculature and microenvironment normalization: a possible mechanism of antiangiogenesis therapy. Cancer Biother Radiopharm. 2008;23:661-7.
48. Huang G, Chen L. Discrepancies between antiangiogenic and antitumor effects of recombinant human endostatin. Cancer Biother Radiopharm. 2009;24:589-96.
49. Rosenberg, SA. Overcoming obstacles to the effective immunotherapy of human cancer. Proc Natl Acad Sci U S A. 2008;105:12643-4.
50. Rolny C, Mazzone M, Tugues S, Laoui D, Johansson I, Coulon C, Squadrito ML, Segura I, Li X, Knevels E, Costa S, Vinckier S, Dresselaer T, Åkerud P, De Mol M, Salomäki H, Phillipson M, Wyns S, Larsson E, Buysschaert I, Botling J, Himmelreich U, Van Ginderachter JA, De Palma M, Dewerchin M, Claesson-Welsh L, Carmeliet P. HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell. 2011;19:31-44.
51. Manning EA, Ullman JG, Leatherman JM, Asquith JM, Hansen TR, Armstrong TD, Hicklin DJ, Jaffee EM, Emens LA. A vascular endothelial growth factor receptor-2 inhibitor enhances antitumor immunity through an immune-based mechanism. Clin Cancer Res. 2007;13:3951-9. (Pubitemid 47037603)
52. Shrimali RK, Yu Z, Theoret MR, Chinnasamy D, Restifo NP, Rosenberg SA. Antiangiogenic agents can increase lymphocyte infiltration into tumor and enhance the effectiveness of adoptive immunotherapy of cancer. Cancer Res. 2010;70:6171-80.
53. Hamzah J, Jugold M, Kiessling F, Rigby P, Manzur M, Marti HH, Rabie T, Kaden S, Gröne HJ, Hämmerling GJ, Arnold B, Ganss R. Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature. 2008;453:410-4. (Pubitemid 351693122)
54. Dings RP, Vang KB, Castermans K, Popescu F, Zhang Y, OudeEgbrink MG, Mescher MF, Farrar MA, Griffioen AW, Mayo KH. Enhancement of T-cell-mediated antitumor response: angiostatic adjuvant to immunotherapy against cancer. Clin Cancer Res. 2011;17:3134-45.
55. Rettinger E, Kuçi S, Naumann I, Becker P, Kreyenberg H, Anzaghe M, Willasch A, Koehl U, Bug G, Ruthardt M, Klingebiel T, Fulda S, Bader P. The cytotoxic potential of interleukin-15-stimulated cytokine-induced killer cells against leukemia cells. Cytotherapy. 2012;14:91-103.